Volume 13, Supplementary Issue, December 2020 ISSN 1995-6673 JJBS Pages 637 - 646 Jordan Journal of Biological Sciences

Landmark-based Morphometric and Meristic Variations in Emperors (, , Percoidei) from Three Areas around Sulawesi (Indonesia) with Different Levels of Destructive Fishing

Muhammad Afrisal1, Nurjirana1, Irmawati1, Yukio Iwatsuki2 and Andi Iqbal Burhanuddin3,*

1Department of Fisheries Science, Faculty of Marine Science and Fisheries, Hasanuddin University, Indonesia; 2 Division of Fisheries Sciences, Faculty of Agriculture, Miyazaki University, Japan. 3 Marine Biology Laboratory, Faculty of Marine Science and Fisheries, Hasanuddin University, Makassar, Indonesia

Received: December 30, 2019; Revised: February 23, 2020; Accepted: April 6, 2020

Abstract

This study analysed the variation in morphometric and meristic characteristics among fishes in the Lethrinus from three areas around Sulawesi (Indonesia) with different levels of destructive fishing: Makassar, South Sulawesi, high; Manado, North Sulawesi, medium; and Wakatobi, Southeast Sulawesi, low. The research was conducted from June- November 2019. Morphometric characters (21) and meristic characters (8) of L. erythropterus, L. semicintus, L. obsoletus, L. ornatus, and L. harak were measured (30 specimens//site). Morphometric characters were compared between areas using one-way analysis of variance (ANOVA) with post-hoc Tukey Test. Characteristic traits and similarities between species/areas were evaluated using Multivariate Discriminant Function Analysis (DFA) test and tree diagram (dendrogram) analysis. For the five lethrinid species studied there were statistically significant differences (P<0.05) in morphometric characters between the Makassar population and the populations in Manado and Wakatobi. Interestingly, meristic count variability was greater in lethrinids from Makassar and Manado compared to those from the Wakatobi marine protected area. Differences in destructive fishing level between areas are one factor influencing lethrinid morphometric and meristic characters, which can also be influenced by other environmental conditions.

Keywords: Sulawesi, morphometric, meristic, destructive fishing, Lethrinidae

uniform between areas (Unsworth et al., 2018; Briggs 1. Introduction (2003) categorised the risk level as high in the waters off Makassar in South Sulawesi, medium in the waters off Emperors (: Lethrinidae) are a group of Manado in North Sulawesi, and low in the waters of the high-value coral reef-associated fishes found in tropical Wakatobi Archipelago in Southeast Sulawesi. The past 44 and sub-tropical waters. Emperors can be found from the years have also seen changes in the coral cover of back-reef area, including shallow seagrass beds, to the reef Sulawesi reefs (Nurdin et al, 2016; Nurdin et al, 2015; crest and slopes to depths of a few hundred meters Edinger et al, 1998). (Carpenter and Allen, 1989). There are approximately 29 Fishing pressure and destructive fishing along with species of emperors in the Family Lethrinidae, of which phenomena associated with global warming are increasing 86% have been reported from Indonesian waters the pressure on fish communities (Andrés et al, 2013). (Carpenter and Randall, 2003; Lo Galbo et al, 2002). The Fishes of the genus Lethrinus are protogynous Lethrinidae are further divided into two subfamilies: the hermaphrodites (Marriott et al, 2010; Motlagh et al, Lethrininae (with a single genus: Lethrinus) and the 2010), changing from female to male after more than five Monotaxinae (genera , and years, at around 33 cm total length (Wassef, 1991). In ). addition to the high fishing mortality of small size classes, The high volume of exports and lack of regulation on global warming phenomena are detrimental to fitness, with the trade in fishes of the genus Lethrinus have given rise to impacts at the population level including imbalance in the concerns regarding the condition of these populations. sex ratio of Lethrinus populations. This imbalance can lead Furthermore, in addition to heavy demand from the export to the emergence of cryptic species which can affect the market, Lethrinus populations are threatened by the population structure in multi-species Lethrinus various destructive fishing methods used to catch these communities, with the potential to severely affect the valuable fish (Briggs, 2003). Destructive fishing is condition and even the survival of these fisheries prevalent in the seas around Sulawesi, but severity is not resources, including changes in morphological characters.

* Corresponding author e-mail: [email protected]; [email protected]. 638 © 2020 Jordan Journal of Biological Sciences. All rights reserved - Volume 13, Supplementary Issue At an intra-species level, however, change in identification, discrimination, and classification of fishery morphological characteristics is not always controlled stocks, and can also indicate differences in growth and principally by genetic factors, but rather by changes in the maturation rates because body form is a product of surrounding environment (Clayton, 1981). Phenotypic ontogeny (Hayward and Margraf, 1987; Roby et al, 1991; plasticity is strategy employed by many fishes to enable Cadrin, 2000). These considerations prompted this them to adapt to their environment through physiological research with the aim of analysing the biodiversity and and behavioural modifications which can lead to or entrain population structure of Lethrinus species in waters around morphological and reproductive changes and alter survival Sulawesi using an approach based on morphometric rates in order to reduce the impacts of environmental characters. The results of this research will contribute to change. Such strategies do not necessarily result in genetic the scientific basis for forming policies and outlining changes within the population, and such morphological effective strategies to manage and conserve Lethrinus differences between populations cannot be used as proof of communities. genetic differences (Meyer, 1987; Stearns, 1983). In the context of stock management for fishes such as 2. Materials and Methods the genus Lethrinus, the analysis of differences in morphometric and meristic characters can enable the This research was carried out from June to November grouping of individuals or populations (Burhanuddin, 2019 in three sea areas around Sulawesi, Indonesia: the 2014). Quantitative morphometric studies are an important waters of Manado City in North Sulawesi Utara; the key to determining sex and species (Brzesky and Doyle, waters off Makassar City in South Sulawesi; and the 1988), describing the patterns of morphological traits waters of the Wakatobi District (Wakatobi Archipelago) in which can differentiate between populations or species Southeast Sulawesi (Figure 1). Samples were collected and (Ballesteros-Córdova et al, 2016; Firawati et al, 2017), in then analysed at the Marine Biology Laboratory, Faculty taxonomic classification and the estimation of of Marine Science and Fisheries, Universitas Hasanuddin, phylogenetic relationships, and in identifying new species in Makassar. (Burhanuddin and Iwatsuki, 2003). Landmark-based morphometric methods are increasingly used in the

Figure 1. Sampling locations for Lethrinid fishes within Sulawesi waters: (A) Manado, North Sulawesi; (B) Makassar, South Sulawesi; (C) Wakatobi, Southeast Sulawesi. The total number of fish sampled was 450 specimens, Hubbs and Lagler (1958) (Table 1, Figure 2), except for belonging to five species of the genus Lethrinus: L. the number of -rakers (Burhanuddin et al, 2002). erythropterus, L. semicintus, L. obsoletus, L. ornatus, and Measurements were made using digital callipers (WIPRO, L. harak. The measurement of morphometric and meristic WP-150B, precision 0.02 mm). characters mostly followed Brzesky and Doyle (1988) and © 2020 Jordan Journal of Biological Sciences. All rights reserved - Volume 13, Supplementary Issue 639 Table 1. Lethrinus morphometric characters measured, based on Brzesky and Doyle (1988).

Body Section Code Character Description A1 Posteriormost point of maxilla to origin of pelvic fin A2 Posteriormost point of maxilla to posteriormost point of eye A3 Posteriormost point of eye to origin of dorsal fin Head A4 Origin of pelvic fin to origin of dorsal fin A5 Posteriormost point of eye to origin of pelvic fin A6 Posteriormost point of maxilla to origin of dorsal fin B1 Origin of pelvic fin to origin of anal fin B3 Origin of dorsal fin to point between spinous and soft portions of dorsal fin Anterior Body B4 Origin of anal fin to point between spinous and soft portion of dorsal fin

B5 Origin of dorsal fin to origin of anal fin B6 Origin of pelvic fin to point between spinous and soft portions of dorsal fin C1 Origin of anal fin to insertion of anal fin C3 Point between spinous and soft portions of dorsal fin to insertion of dorsal fin Posterior C4 Insertion of anal fin to insertion of dorsal fin Body C5 Point between spinous and soft portions of dorsal fin to insertion of anal fin C6 Origin of anal fin to insertion of anal fin D1 Insertion of anal fin to anterior attachment of ventral membrane from caudal fin D3 Insertion of dorsal fin to anterior attachment of dorsal membrane from caudal fin Tail Anterior attachment of ventral membrane from caudal fin to anterior attachment of dorsal D4 membrane from caudal fin D5 Insertion of dorsal fin to anterior attachment of ventral membrane from caudal fin D6 Insertion of anal fin to anterior attachment of dorsal membrane from caudal fin The meristic characters counted were: (1) Dorsal fin-rays, (2) variance (ANOVA) followed by post-hoc Tukey tests. Anal fin-rays, (3) Pectoral fin-rays, (4) Pelvic fin-rays, (5) Lateral Further analysis using Multivariate Discriminant Function line scales, (6) Scales above lateral line, (7) Scales below lateral Analysis (DFA) was used to identify characters specific (to line, and (8) number of gill-rakers. a species or site), and resemblances between species or sites. These analyses were implemented in SPSS version 22.0. Principal Component Analysis (PCA) and tree (dendrogram) analysis were used to analyse the patterns of diversity between species at each site; these analyses were implemented in Minitab version 17.0.

3. Results

3.1. Morphometric Characters of Lethrinus spp. Figure 2. Morphometric truss for the genus Lethrinus, showing The measurements of the morphometric characters of the location of the 10 anatomical points (landmarks) used and the Lethrinus spp. species are given in Table 2. The results of morphometric distances measured for each individual (Brzesky the one-way analysis of variance followed by Tukey post- and Doyle, 1988). hoc tests (at 95% confidence level) are also shown in this Before analysing the morphometric data, the data were table. The principle component analysis eigenvalues and standardised using the regression from Elliot et al. (1995). coefficients are shown in Table 3. A scatterplot of the This model was used to remove the size component from specimens along the first and second axes (roots) of the the measurements of shape and homogenise the variation principle components analysis results is shown in Figure 3. within the sample (Jolicoeur, 1963). The regression The Discriminant Function Analysis (DFA) assignment of formula from Elliot et al. (1995) is: each specimen is shown in Table 4. 3.1.1. Lethrinus erythropterus Ms = Mo The majority of the 21 characters were observed where M s is the standardized measurement of the character, Mo is the original morphometric measurement (mm), Ls is the standard significantly (P< 0.05) for L. erythropterus with the length of the fish, and Lt the mean of the standard length of all fish exception of the character A3 (the posteriormost point of from all samples. The parameter b was estimated for each the eye to the origin of the dorsal fin); however, there was character from the observed data as the slope of the regression of significant grouping of L. erythropterus populations by site log M on log L, using all specimens. (Table 2). The Manado and Wakatobi populations The standardised morphometric data for the 450 resembled each other for the characters A2, A6, B1, B3, specimens was compared using One-Way analysis of B4, C1, and C4. The Makassar L. erythropterus population 640 © 2020 Jordan Journal of Biological Sciences. All rights reserved - Volume 13, Supplementary Issue differed from the other two locations for morphometric However, the difference was not significant between the characters A4, A5, B5, B6, C3, C5, C6, D1, D3, D4, D5, Manado and Wakatobi populations for characters A2, B3, and D6. B6, C1, C3, C5, D1, D3, D6, and between the Manado and Standardized coefficients of canonical variables (roots) Makassar populations for characters A1, A3, and C4. 1 and 2 from the DFA showed 95.4% and 41.7% variation The standardized coefficients of canonical variables between the populations analysed, with 20 principal (roots) 1 and 2 from the DFA for L. obsoletus showed variables for discriminating between groups (Table 3). In 90.25% and 49% variation between the populations canonical root 1, the variables with major effects were: A6 analysed, with 22 principal discriminant group variables. (Y=1.304), B1 (Y=0.659), B3 (Y=0.323), B5 (Y=0.674), The variables with the greatest influence on Root 1 were: C3 (Y=0.782), C5 (Y=-0.362), C6 (Y=-0.365), D4 (Y=- A1 (Y=0.587), A3 (Y=0.310), A4 (Y=0.318), A6 0.373), (Y=0.713), D6 (Y=0.713). For root 2, variables (Y=0.520), B1 (Y=0.544), B5 (Y=0.645), C1 (Y=0.621), with major effects were: A2 (Y=-0.388), A3 (Y=-0.423), C4 (Y=-0.449), D1 (Y=0.379), D3 (Y=0.672), D6 A4 (Y=-0.564), A5 (Y=1.328), B5 (Y=-0.347), C3 (Y=0.347). The variables with the greatest influence on (Y=0.354), C4 (Y=-0.473), C5 (Y=0.391), D1 (Y=0.504), Root 2 were: A2 (Y=0.587), A3 (Y=0.516), A4 (Y=0.988), D3 (Y=0.495), D4 (Y=-538). A5 (Y=-1.072), B5 (Y=0.687), C3 (Y=-0.562), C4 Predictive classification assigned 93.3% of the 90 L. (Y=0.625), C5 (Y=-0.509), D4 (Y=0.572), D5 (Y=-0.443). erythropterus specimens to their population of origin Predictive classification assigned 94.4% of the 90 L. (Table 4). The L. erythropterus collected from Manado obsoletus sampled to their population of origin (Table 4). contained 3 specimens assigned to the Wakatobi group and Two individuals from the Manado L. obsoletus population vice-versa. Meanwhile, the L. erythropterus from were assigned to the Wakatobi population, and vice-versa. Makassar formed a distinct group (100% assignment to One individual from the Makassar population was place of origin) . assigned to the Manado group. 3.1.2. Lethrinus semicintus 3.1.4. Lethrinus ornatus The one-way ANOVA showed that certain characters The one-way ANOVA showed a significant (P < 0.05) contributed significantly (p<0.05) to between population between-site difference for the 21 morphometric differences in L. semicintus (Table 2). The Tukey post-hoc characters. The Tukey post-hoc test did not show test showed significant differences between populations, significant variation between the Manado and Wakatobi except for the character C1, the origin of the anal fin to the populations of L. ornatus for characters A1, A2, A3, B1, insertion of the anal fin (P > 0.05). The Manado and C1, C3, C5, D1, D3, D5, D6, while for character D4 the Wakatobi populations were similar for the characters A1, difference between Makassar and Wakatobi populations A2, A5, B4, B5, C4, C5, C6, D1, D3, D4, D5, and D6. The was not significant. However, nine characters differed Makassar population was significantly different from the significantly between all three populations (A4, A5, A6, other two populations for characters A3, A4, A6, B1, B3, B3, B4, B5, B6, C4, and C6). B6, while character C3 was similar for the Makassar and The standardized coefficient of DFA canonical Wakatobi populations (Table 2). variables (roots) 1 and 2 showed 90.25% and 32.49% The standardized coefficients of the canonical variable variation between the three L. ornatus populations, with 14 (root) 1 and 2 obtained from the DFA show 96.04% and principal discriminant variables. The morphometric 50.41% variation between the populations analysed, with characters influencing Root 1 were: A6 (Y=0.934), B1 19 principal variables for discriminating between groups (Y=0.443), B4 (Y=-0.517), B6 (Y=0.353), C4 (Y=-0.370), (Table 3). The morphometric characters influencing root 1 C6 (Y=0.568), D1 (0.526). The characters with the greatest where: A4 (Y=-0.316), A6 (Y=1.078), B1 (Y=0.744), B5 influence on Root 2 were: A1 (Y=0.342), B1 (Y=0.340), (Y=0.587). The variables with the strongest influence on B6 (Y=-0.560), C1 (Y=0.408), C3 (Y=0.332), C6 (-0.370), root 2 were: A2 the posteriormost point of the maxilla to and D3 (Y=0.409). the posteriormost point of the eye (Y=-0.840), A3 (Y=- Predictive classification assigned 95.6% of the 90 L. 0.448), A4 (Y=0,541), A6 (Y=0.322), B1 (Y=0.336), B5 ornatus individuals to their site of origin (Table 4). The (Y=0.683), B6 (Y=-0.895), C1 (Y=0.482), C4 (Y=-0.317), Manado population of L. ornatus (93.3%) had 2 D1 (Y=0.333), D3 (Y=868), D4 (Y=0.542), D5 (Y=- individuals assigned to the Wakatobi group and vice-versa. 0.531), D6 (Y=-0.565). The Makassar population formed a distinct group with Predictive classification of individuals showed an 100% assignment to site of origin. overall 97.8% assignment of L. semicintus to population of 3.1.5. origin (Table 4). The DFA assigned one individual from the Manado population of L. semicintus to the Wakatobi The one-way ANOVA of the 21 morphometric population and vice-versa, while the L. semicintus characters L. harak showed significant (P< 0.05) population from Makassar clustered apart from the other differences between the three populations at the 95% two populations with 100% assignment to site of origin. confidence level, indicating a significant effect of population on shape for this species. The Tukey post-hoc 3.1.3. test (Table 2) showed that the Manado and Wakatobi The ANOVA showed a significant (p<0.05) effect of population had similar values for seven characters (A1, population (site) on morphometric characters; the Tukey A3, B1, B3, C4, D1, and D4), while Makassar and post-hoc test determined the level of significance for each Wakatobi populations had similar values for three parameter (Table 2). There was a significant difference (P characters (C1, C3, and C5); however, character D3 < 0.05) between the three L. obsoletus populations for differed significantly between the Makassar and Wakatobi eight characters (A4, A5, A6, B1, B5, C6, D4, and D5). populations. The values of ten characters (A2, A4, A5, A6, © 2020 Jordan Journal of Biological Sciences. All rights reserved - Volume 13, Supplementary Issue 641 B4, B5, B6, C6, D5, and D6) differed significantly B1 (Y=0.340), B3 (Y=-0.323), B6 (Y=-0.560), C1 between all three species. (Y=0.408), C3 (Y=0.332), C6 (Y=-0.370), and D3 The standardized coefficients of canonical components (Y=0.409). (roots) 1 and 2 from the DFA explained 90.25% and Predictive classification assigned 91.1% of the 90 L. 32.49% of between population variation, with 14 principal harak individuals to their site of origin (Table 4). From the discriminant group variables (Table 3). The morphometric Manado population, one individual was assigned to the characters influencing Root 1 values were: A6 (Y=0.934), Wakatobi population. From the Wakatobi population, four B1 (Y=0.443), B4 (Y=-0.517), B6 (Y=0.353), C4 (Y=- individuals were assigned to Manado and one to Makassar. 0.370), C6 (Y=0.568), and D1 (Y=0.526). The main Two individuals from Makassar were assigned to the characters influencing Root 2 values were: A1 (Y=0.342), Wakatobi group. Table 2. Variation (mean and standard deviation) in the morphometric characters of Lethrinus spp. from Sulawesi, Indonesia

L. erythropterus L. semicintus L. obsoletus L. ornatus L. harak Code Manado Makassar Wakatobi Manado Makassar Wakatobi Manado Makassar Wakatobi Manado Makassar Wakatobi Manado Makassar Wakatobi A1 46.33 ± 2.69a 51.69 ± 2.10b 48.30 ± 4.36c 47.37 ± 7.60a 50.27 ± 1.69b 45.89 ± 2.39a 47.55 ± 1.45a 48.56 ± 2.05a 46.24 ± 2.35b 41.84 ± 1.46a 45.05 ± 2.26b 41.55 ± 2.01a 44.68 ± 3.57a 48.81 ± 2.21b 45.89 ± 2.58a A2 57.64 ± 3.47a 64.60 ± 2.74b 58.06 ± 3.04a 49.61 ± 2.75a 55.37 ± 1.21b 49.03 ± 2.19a 50.32 ± 3.49a 52.94 ± 1.50b 49.39 ± 1.44a 50.40 ± 2.80a 56.12 ± 2.17b 49.21 ± 2.11a 47.22 ± 3.86a 53.40 ± 1.76b 49.82 ± 2.20c A3 26.17 ± 8.76a 28.44 ± 1.98a 25.49 ± 1.91a 22.49 ± 3.35a 25.31 ± 1.44b 20.93 ± 1.75c 26.78 ± 6.67a 25.90 ± 1.53a 23.17 ± 1.32b 23.41 ± 1.62a 25.47 ± 2.12b 22.40 ± 2.46a 26.17 ± 4.21a 30.10 ± 1.91b 26.98 ± 2.77a A4 72.72 ± 2.03a 83.75 ± 3.44b 75.40 ± 3.70c 57.96 ± 1.71a 64.07 ± 2.40b 56.55 ± 2.23c 63.92 ± 1.29a 65.59 ± 1.88b 61.93 ± 2.27c 65.96 ± 1.87a 70.60 ± 2.92b 62.89 ± 1.91c 61.36 ± 5.05a 69.88 ± 3.24b 64.69 ± 3.69c A5 69.15 ± 1.93a 77.97 ± 2.30b 71.80 ± 3.64c 56.86 ± 1.85a 62.70 ± 2.11b 55.78 ± 1.68a 61.34 ± 1.44a 62.91 ± 1.33b 60.25 ± 1.85c 63.12 ± 1.73a 67.60 ± 2.16b 60.92 ± 1.83c 59.51 ± 5.32a 67.21 ± 2.47b 62.61 ± 3.33c A6 74.49 ± 4.93a 86.77 ± 2.39b 75.89 ± 3.94a 65.39 ± 2.30a 74.34 ± 1.58b 64.21 ± 1.69c 69.52 ± 2.55a 73.50 ± 2.13b 66.86 ± 1.72c 67.11 ± 1.86a 74.36 ± 2.45b 64.61 ± 1.65c 66.46 ± 5.48a 75.09 ± 2.45b 69.15 ± 3.84c B1 53.64 ± 3.45a 58.90 ± 4.35b 53.84 ± 2.93a 48.93 ± 3.51a 52.08 ± 2.77b 46.92 ± 2.21c 50.74 ± 2.21a 54.44 ± 2.89b 49.13 ± 2.17c 46.57 ± 2.57a 48.64 ± 3.11b 45.57 ± 2.45a 49.49 ± 3.98a 56.63 ± 2.91b 51.38 ± 2.53a B3 58.67 ± 2.37a 65.86 ± 2.35b 59.34 ± 3.21a 52.63 ± 1.93a 58.61 ± 3.63b 49.72 ± 2.66c 54.08 ± 1.41a 56.07 ± 1.23b 53.21 ± 2.25a 52.97 ± 1.65a 55.73 ± 2.00b 50.87 ± 1.76c 52.60 ± 3.73a 57.44 ± 1.73b 53.79 ± 3.44a B4 67.24 ± 1.79a 76.56 ± 2.79b 69.47 ± 5.40a 50.78 ± 1.29a 55.92 ± 1.25b 50.32 ± 1.79a 58.76 ± 1.22a 59.80 ± 1.80ab 56.42 ± 7.37ac 60.73 ± 1.54a 64.63 ± 2.74b 59.24 ± 2.00c 56.94 ± 4.44a 64.55 ± 1.90b 61.33 ± 3.84c B5 88.50 ± 1.92a 101.06 ± 3.13b 90.62 ± 3.51c 73.14 ± 4.68a 81.00 ± 1.50b 72.43 ± 1.68a 80.92 ± 1.63a 83.11 ± 1.41b 79.16 ± 1.91c 81.07 ± 1.17a 85.34 ± 3.98b 78.94 ± 1.67c 78.38 ± 5.54a 86.84 ± 2.19b 82.22 ± 4.24c B6 89.76 ± 1.98a 101.10 ± 4.07b 91.97 ± 3.44c 74.08 ± 1.86a 80.87 ± 2.40b 70.93 ± 2.18c 79.77 ± 1.78a 82.97 ± 2.13b 78.66 ± 3.30a 80.11 ± 3.01a 84.33 ± 2.89b 76.18 ± 1.69c 77.61 ± 5.98a 88.52 ± 2.80b 81.22 ± 4.54c C1 34.80 ± 3.09a 39.05 ± 3.06b 36.23 ± 1.74a 31.41 ± 9.57a 33.38 ± 1.01a 30.15 ± 1.01a 32.64 ± 0.77a 33.85 ± 0.86b 32.35 ± 0.89a 32.48 ± 1.23a 34.93 ± 1.21b 32.86 ± 5.24a 32.96 ± 2.98a 36.54 ± 1.37b 35.85 ± 2.07b C3 31.95 ± 0.96a 36.61 ± 2.46b 34.83 ± 3.25c 29.85 ± 2.38a 32.47 ± 1.49b 32.41 ± 3.27b 31.98 ± 0.85a 33.08 ± 0.79b 32.46 ± 1.31a 32.99 ± 1.01a 34.58 ± 2.15b 33.08 ± 1.94a 32.58 ± 2.80a 37.01 ± 0.92b 37.45 ± 3.33b C4 32.97 ± 1.47a 37.24 ± 1.54b 33.36 ± 1.59a 28.14 ± 4.01a 30.21 ± 3.32b 26.35 ± 0.92a 30.64 ± 0.86a 30.96 ± 1.01a 29.91 ± 1.09b 29.33 ± 0.91a 30.77 ± 1.20b 28.51 ± 1.04c 29.83 ± 2.86a 32.79 ± 1.97b 31.04 ± 1.95a C5 57.73 ± 1.63a 65.36 ± 2.48b 60.48 ± 3.21c 48.20 ± 1.01a 52.69 ± 1.12b 49.16 ± 2.42a 54.34 ± 1.02a 55.36 ± 1.32b 54.10 ± 1.57a 54.92 ± 1.36a 57.74 ± 2.30b 53.99 ± 2.09a 53.26 ± 4.12a 60.63 ± 1.30b 58.97 ± 3.83b C6 58.03 ± 1.29a 65.56 ± 2.56b 61.14 ± 8.25c 47.14 ± 0.90a 52.35 ± 1.38b 46.58 ± 1.41a 52.63 ± 1.14a 54.37 ± 1.72b 51.76 ± 1.18c 52.46 ± 1.11a 55.70 ± 1.70b 50.72 ± 1.46c 51.60 ± 4.70a 57.90 ± 1.15b 55.17 ± 4.01c D1 26.42 ± 2.26a 32.70 ± 2.61b 29.00 ± 1.89c 28.70 ± 1.77a 31.87 ± 1.99b 28.64 ± 2.44a 28.39 ± 1.59a 31.32 ± 1.69b 28.41 ± 1.49a 26.40 ± 1.59a 28.78 ± 1.74b 25.95 ± 1.16a 29.91 ± 3.28a 33.12 ± 2.28b 30.86 ± 2.36a D3 26.36 ± 2.04a 30.04 ± 1.81b 28.75 ± 2.37c 27.07 ± 1.89a 29.31 ± 1.70b 28.10 ± 2.19a 27.30 ± 1.74a 30.48 ± 1.48b 27.99 ± 1.42a 25.99 ± 2.12a 28.55 ± 2.42b 26.58 ± 1.73a 29.07 ± 2.84a 31.13 ± 2.07b 30.13 ± 2.17ab D4 25.19 ± 1.35a 29.03 ± 1.33b 26.17 ± 1.21c 19.61 ± 0.83a 22.69 ± 1.20b 19.95 ± 0.99a 23.45 ± 0.82a 24.61 ± 0.71b 22.75 ± 0.77c 22.64 ± 5.68a 23.38 ± 1.01ab 21.08 ± 0.87ac 22.46 ± 2.21a 25.51 ± 1.21b 23.27 ± 2.12a D5 38.26 ± 1.55a 44.33 ± 1.92b 40.24 ± 2.50c 35.43 ± 1.87a 38.99 ± 1.04b 34.50 ± 1.75a 37.73 ± 1.01a 40.74 ± 1.42b 37.82 ± 1.45c 35.55 ± 1.67a 38.84 ± 1.45b 35.30 ± 1.83a 37.67 ± 3.49a 42.27 ± 2.01b 39.66 ± 2.83c a b c a b a a b a a b a a b a D6 39.91 ± 1.57 46.57 ± 2.25 41.73 ± 1.49 37.15 ± 1.45 40.64 ± 1.41 36.54 ± 1.43 39.11 ± 1.76 42.12 ± 1.58 38.28 ± 1.30 35.97 ± 2.13 39.09 ± 1.88 35.42 ± 1.01 39.71 ± 3.42 43.67 ± 2.12 40.23 1.99 *One-way ANOVA with Tukey post-hoc test; different superscript letters indicate significant difference at α= 0.05 Table 2. Eigenvalue, cumulative variance (%), canonical correlation, and standardized coefficients of the canonical variables produced by the principle components analysis of morphometric characters for Lethrinus species from Sulawesi, Indonesia Species L. erythropterus L. semicintus L. obsoletus L. ornatus L. harak Discriminant Variables Function Function Function Function Function 1 2 1 2 1 2 1 2 1 2 Eigenvalue 21.127 0.71 24.46 1.02 10.47 0.98 11.20 0.49 11.2 0.49 Cumulative% of variance 96.7 3.3 96 4 91.4 8.6 95.8 4.2 95.8 4.2 Canonical correlation 0.977 0.646 0.98 0.71 0.95 0.70 0.95 0.57 0.95 0.57 A1 .001 -.130 .249 -.083 .587 .070 .185 .342 .185 .342 A2 .264 -.388 -.241 -.840 .140 .587 .263 .198 .263 .198 A3 .678 -.423 -.071 -.448 .310 .516 .130 -.272 .130 -.272 A4 -.183 -.564 -.316 .541 .318 .988 -.273 -.106 -.273 -.106 A5 .199 1.32 -.251 -.012 -.248 -1.072 .062 .007 .062 .007 A6 1.304 -.024 1.078 .322 .520 .014 .934 .006 .934 .006 B1 .659 .149 .744 .336 .544 -.053 .443 .340 .443 .340 B3 .323 -.280 .128 -.010 -.244 -.270 .212 -.323 .212 -.323 B4 -.268 .092 -.024 -.085 -.203 -.111 -.517 .291 -.517 .291 B5 .674 -.347 .587 .683 .645 .687 .004 .100 .004 .100 B6 -.188 .090 .069 -.895 .058 -.294 .353 -.560 .353 -.560 C1 .189 .087 .717 .482 .621 -.267 -.049 .408 -.049 .408 C3 .782 .354 .165 .154 .250 -.562 .002 .332 .002 .332 C4 -.227 -.473 -.021 -.317 -.449 .625 -.370 -.041 -.370 -.041 C5 -.362 .391 -.060 .254 -.453 -.509 -.154 -.227 -.154 -.227 C6 -.365 .021 .508 .206 -.151 -.094 .568 -.370 .568 -.370 D1 .177 .504 .153 .333 .379 -.043 .526 .241 .526 .241 D3 -.216 .495 .157 .868 .672 -.021 .129 .409 .129 .409 D4 -.373 -.538 .156 .542 -.167 .572 .043 -.259 .043 -.259 D5 .270 .078 .289 -.531 -.002 -.443 .067 .197 .067 .197 D6 .713 -.109 -.002 -.565 .347 -.282 -.149 .246 -.149 .246 642 © 2020 Jordan Journal of Biological Sciences. All rights reserved - Volume 13, Supplementary Issue

Table 4. Predictive classification of individuals for five Lethrinus species from Sulawesi Collection Number of specimens assigned Assignment (%) Species site Manado Makassar Wakatobi Manado Makassar Wakatobi L. Manado 27 0 3 90.0 0.0 10.0 erythropterus Makassar 0 30 0 0.0 100.0 0.0 Wakatobi 3 0 27 10.0 0.0 90.0 L. Manado 29 0 1 96.7 0.0 3.3 semicinctus Makassar 0 30 0 0.0 100.0 0.0 Wakatobi 1 0 29 3.3 0.0 96.7 L. obsoletus Manado 28 0 2 93.3 0.0 6.7 Makassar 1 29 0 3.3 96.7 0.0 Wakatobi 2 0 28 6.7 0.0 93.3 L. ornatus Manado 28 0 2 93.3 0.0 6.7 Makassar 0 30 0 0.0 100.0 0.0 Wakatobi 2 0 28 6.7 0.0 93.3 L. harak Manado 29 0 1 96.7 0.0 3.3 Makassar 0 28 2 0.0 93.3 6.7 Wakatobi 4 2 25 13.3 6.7 83.3 3.1.6. Graphical analyses of morphometric characters mostly grouped in the upper right-hand quadrant, while L. semicintus predominantly grouped in the lower left-hand The distribution of the specimens along PCA quadrant, L. obsoletus straddled the lower right and left components (roots) 1 and 2 based on morphometric quadrants, L. ornatus mostly grouped in the upper left- characters indicates a close relationship between the five hand quadrant, and L. harak straddled the upper and lower Lethrinus species (Fig. 3), with considerable overlap right-hand quadrants. between species. In general, L. erythropterus specimens

5 L. erythropterus Manado L. erythropterus Makassar 4 L. erythropterus Wakatobi L. semicintus Manado 3 L. semicintus Makassar

t L. semicintus Wakatobi

n L. obsoletus Manado e 2

n L. obsoletus Makassar o

p 1 L. obsoletus Wakatobi

m L. ornatus Manado o

C L. ornatus Makassar 0

d L. ornatus Wakatobi n

o L. harak Manado

c -1

e L. harak Makassar

S L. harak Wakatobi -2

-3

-4

-20 -15 -10 -5 0 5 10 First Component Figure 3. Scatterplot of the 420 specimens from three study locations and five species of the genus Lethrinus on the first component (Root 1) and second component (Root 2) of the principal component analysis based on 21 morphometric variables.

The tree analysis of the 21 morphometric variables (Fig. 4) shows distinct groupings based on the combination 0.00 of species and study location. At the 66.67% level of similarity, four groups were formed: (1) L. erythropterus y t

Manado, L. erythropterus Wakatobi, L. harak Makassar, L. i 33.33 r a l ornatus Makassar; (2) L. erythropterus Makassar; (3) L. i m i semicintus Manado, L. semicintus Wakatobi; (4) L. S semicintus Makassar, L.obsoletus Makassar, L. obsoletus 66.67 Manado, L. obsoletus Wakatobi, L. harak Manado, L. harak Wakatobi, L. ornatus Manado, L. ornatus Wakatobi. 100.00 i r r r i r r i i i o b a a a o b a a o b o b o b Despite this somewhat unexpected structure, for each of d s s s d s s d d d a to s s s a to s s a to a to a to n a a a a n a a a n a n a n a a k k k k a k k k a k a k a k a a a a a a a a a a M M M M M the five species the Manado and Wakatobi populations s W M M M s W M M s W k W s W u s k s s u s s s u s a u s r a u u t u u t r k t e ru r t r in tu t t le tu a ra a tu t e a a e c n in le e h a n a were relatively closely grouped with each other, but were p t h n t i i c o l . r n o p . r p ic i o s o L h o r r o L o o m s b s L. . o h r . r e m m b o b L . t h L t s e e o . o L ry t h L. s s . L . not closely grouped with conspecifics from Makassar. e y ry . . L L . r e L L L e . L. L Observations Figure 4. Dendrogram based on the similarity (Euclidean distance) of the 21 morphometric variables measured for five Lethrinus species from three study locations. © 2020 Jordan Journal of Biological Sciences. All rights reserved - Volume 13, Supplementary Issue 643 The canonical discriminant function analysis of group The centroid positions indicate that the first component centroids showed a similar grouping pattern for the five predominantly discriminates between the Makassar species (Fig. 5). The Manado and Wakatobi specimens population and the other two populations, while the second tended to be grouped to the left of the vertical axis, above component predominantly discriminates between the or below the horizontal axis. Conversely, the Makassar Wakatobi and Manado populations. populations were grouped to the right of the vertical axis.

Figure 5. Distribution of the three Lethrinus populations studied based on discriminant analysis of morphometric characters for five species: (A) L. erythropterus: (B) L. semicintus: (C) L. obsoletus: (D) L. ornatus: (E) L. harak.

3.2. Meristic Character Manado and Wakatobi populations. Conversely, the scales above lateral line count varied more in the Manado The counts for the 8 meristic characters (Table 5) show population (4-6) compared to the other two populations. that for four characters the five Lethrinus species had the The number of scales below the lateral line was also more same count range in all three study locations. These varied in Makassar (14-17) compared to the Manado and characters were: anal fin-rays, pectoral fin-rays, pelvic fin- Wakatobi populations which both had the same range (14- rays, and number of gill-rakers. The dorsal spine count 16). differed for L. obsoletus from Wakatobi with two values For L. semicintus, the Manado population had the (IX, X), while for the remaining species and locations the widest range of lateral line scale count (46-50). The dorsal spine count was always ten (X). The remaining number of scales above the lateral line was most varied in three meristic counts (scales above lateral line, scales the Wakatobi population (5-7), followed by Manado and above lateral line, and scales below lateral line) varied Makassar. The scales below the lateral line count varied between species and/or site. more in Manado (13-17) followed by Wakatobi, with once Lateral line scale count varied more for L. again the lowest variation in Makassar. erythropterus from Makassar (42-48) compared to the Table 5. Meristic characters of Lethrinus species from Sulawesi Lateral Anal fin- Pectoral fin- Pelvic fin- Scales above Scales below Number of Species Locality Dorsal fin-rays line rays rays rays lateral line lateral line gill-rakers scales Manado X, 10 III, 9 12 I, 5 44-47 4, 6 14-16 4 L. erythropterus Makassar X, 10 III, 9 12 I, 5 42-48 4, 5 14-17 4 Wakatobi X, 10 III, 9 12 I, 5 44-47 5, 6 14-16 4 Manado X, 10 III, 9 12 I, 5 46-50 5, 6 13-17 4 L. semicintus Makassar X, 10 III, 9 12 I, 5 46-49 4, 5 13-14 4 Wakatobi X, 10 III, 9 12 I, 5 46-49 5, 7 13-16 4 Manado X, 10 III, 9 12 I, 5 45-48 5, 7 14-16 4 L. obsoletus Makassar X, 10 III, 9 12 I, 5 46-48 5 14-15 4 Wakatobi IX, X, 10 III, 9 12 I, 5 46-48 5, 6 14-16 4 Manado X, 10 III, 9 12 I, 5 45-48 5, 6 13-15 4 L. ornatus Makassar X, 10 III, 9 12 I, 5 45-47 5 14-15 4 Wakatobi X, 10 III, 9 12 I, 5 46-48 4, 6 13-16 4 Manado X, 10 III, 9 12 I, 5 43-49 5, 6 13-16 4 L. harak Makassar X, 10 III, 9 12 I, 5 43-48 5, 6 14-15 4 Wakatobi X, 10 III, 9 12 I, 5 45-48 5, 6 14-16 4 644 © 2020 Jordan Journal of Biological Sciences. All rights reserved - Volume 13, Supplementary Issue

The meristic counts for L. obsoletus were most varied revealed that L. nebulosus harvested in the Southwest in Manado, and least varied in Makassar. In Manado, the comprised in fact two cryptic species lateral line scale count range was 45-48, while scales (Healey et al, 2018b). The emergence of cryptic species is above lateral line count range was 5-7. For the latter thought to occur due to various reasons, including character, the Makassar population was homogenous, with topography (Krakau 2008), anthropogenic activity and all specimens having 5 scales above the lateral line. The food availability (Irmawati et al, 2018). range of scales below lateral line count was the same for The growth parameters have been calculated for Manado and Wakatobi (14-16), wider than for Makassar Lethrinus species from different fishing grounds, including (14-15). Southern Iran (Motlagh et al, 2010), the Gulf of Aden For L. ornatus, the range of lateral line scales was (Mehanna et al, 2014), the Persian Gulf (Raeisi et al, greatest in Manado (45-48), and lowest in Wakatobi. 2011), the Egyptian Red Sea (Zaahkouk et al, 2017), and Conversely, the Wakatobi population had the highest within Indonesia in the Thousand Islands (Sevtian, 2012), variation in scales above lateral line (4-6), and scales Spermonde Archipelago (Budimawan et al, 2002), and below lateral line (13-16), with the Makassar population Outer Kendari Bay (Nurdiansyah et al, 2017). For most of having the lowest variation in both these counts. these populations, the growth pattern was allometric For L. harak, scales above lateral line had the same negative, with the exception of the Egyptian Red Sea, and range (5-6) at all three sites. Lateral line scale count and Outer Kendari Bay populations which had isometric scales below lateral line count varied most in the Manado growth patterns. The availability of food is a crucial factor population (43-49 and 13-16), followed by Makassar for in determining growth patterns, and can lead to the former count and Wakatobi for the latter. morphological changes in fish (Clabaut et al, 2007). The results of this study indicate that destructive 4. Discussion fishing may be a key driver of change in the morphometric characters of lethrinids in the waters around Sulawesi, and The one-way analysis of variance (ANOVA) followed therefore that morphometric characters could serve as by Tukey post-hoc test and discriminant function analysis indicators of pressure from destructive fishing. Although (DFA) showed that for most characters measured the destructive fishing activities may not affect individual difference between the Manado and Wakatobi populations lethrinids directly, there are several ways in which they was not significant (P > 0.05), while the Makassar could affect morphological characters. For example, the population differed significantly for most characters (P < explosives used to catch fish can destroy around 0.5 – 2 m2 0.05). The principal components analysis (PCA) and tree per 1 kg of “fish bomb” (McManus et al, 1997; Pet-Soede (dendrogram) analysis gave a similar result, showing close & Erdman, 1998). Destructive fishing can also cause mass groupings of the Manado and Wakatobi populations, with mortality of fish and other marine organisms, which can the Makassar population distinctly separate. lead to a reduction in biodiversity, local extinctions, and a The similarity in characters between Manado and reduction in predators, entraining changes in trophic Wakatobi, and difference with Makassar could be related structure as well as habitat modification (Bacalso and to the differences in fishing pressure at each location. Wolff, 2014; Cinner, 2009). Degradation of coral reefs can While there is a risk of destructive fishing in all waters promote increased algal growth, increasing food around Sulawesi, the frequency is highest in Makassar, availability for herbivores while reducing the abundance of South Sulawesi Selatan, followed by Manado, North potential prey for carnivorous fishes (Piazzi et al, 2012). Sulawesi, and lowest in the Wakatobi, Southeast Sulawesi Such changes will affect the food and feeding habitats of Tenggara (Briggs, 2003). the carnivorous lethrinids (Cinner, 2009). These factors However, change in the dorsal fin-ray count of the can induce modifications in the physiology, reproductive species L. obsoletus was detected in the Wakatobi, the patterns and feeding habit of fishes, which in turn can study location with the lowest level of destructive fishing. induce changes in fish body shape, such as bodily Differences in morphometric and meristic characters can proportions and spine/ray counts (Alonzo et al, 2008; occur in populations of fish which are of the same species Unsworth et al, 2007), as observed in the five lethrinids in but live in different locations (Firawati et al, 2017). this study. Morphological changes in Lethrinus have been reported by Afrisal et al (2018) who found changes in the 5. Conclusion morphological characters of L. erythropterus in the Spermonde Archipelago, Makassar City, in particular For all five species of the genus Lethrinus included in spinal malformations. this study, the Manado and Wakatobi populations were Morphometric variation can be associated with or similar, with little between-population variation in related to genetic variation (Hebert et al, 2003). Genetic morphometric characters, while the Makassar populations analysis and research on parallel genetic structuring in the differed substantially from the other two populations. The southwest Indian Ocean using the cytochrome c oxidase meristic scale counts (scales along lateral line, scales subunit I (COI) mtDNA gene and microsatellites (Healey above lateral line, and scales below lateral line) varied et al, 2018a) found cryptic species within the genus most in the Manado populations and least in Wakatobi Lethrinus, with different populations of some species populations. Differences in destructive fishing levels could (including L. harak, L. mahsena and L. nebulosus) be associated with differences in morphometric characters. appearing to be in fact different species. The species L. The Lethrinus populations within the Wakatobi National harak in this study is strongly divided based on Park, exposed to the lowest level of destructive fishing, morphometric traits, as shown in the tree analysis had less variation in meristic characters compared to the dendrogram (Figure 4). Similarly, genetic research other two populations and some individuals of L. obsoletus © 2020 Jordan Journal of Biological Sciences. All rights reserved - Volume 13, Supplementary Issue 645 had one less spine in the dorsal fin compared to other Carpenter KE and Randall JE. 2003. Lethrinus ravus, a new Lethrinus populations and species. species of emperor fish (Perciformes: Lethrinidae) from the Western Pacific and Eastern Indian Oceans. Zootaxa, 240: 1–8. 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